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Contributors

Fahad H. Abduljabbar, MBBS, FRCSC

Spine Fellow McGill Scoliosis and Spine Centre McGill University Health Centre Montreal, Quebec, Canada Orthopaedic Teaching Assistant Department of Orthopedic Surgery King Abdulaziz University Jeddah, Saudi Arabia

H. Davis Adkisson, PhD

Chief ScientiﬁcOfﬁ cer Isto Biologics St. Louis, Missouri

Mauro Alini, PhD

Head, Musculoskeletal Regeneration Program AO Research Institute Davos Davos, Switzerland

Howard An, MD

The Morton International Professor Director of Spine Fellowship Department of Orthopaedic Surgery Rush University Medical Center Chicago, Illinois

Lorin Michael Benneker, MD

Head of Spine Unit Associate Professor Department of Orthopaedic Surgery Inselspital University of Bern Bern, Switzerland

Robby D. Bowles, PhD

Assistant Professor Department of Bioengineer ing University of Utah Salt Lake City, Utah

Jason Pui Yin Cheung, MBBS (HK), MMedSc

Clinical Assistant Professor, Division of Spine Surgery Department of Orthopaedics & Traumatology The University of Hong Kong Pokfulam, Hong Kong

Kenneth M.C. Cheung, MBBS(UK),MD (HK), FRCS,FHKCOS,

FHKAM(Orth)

Jessie Ho Professor in Spine Surgery, Head, Department of Orthopaedics and Traumatology The University of Hong Kong Hong Kong, SAR, China

Michelle A. Cruz, BS

MD, PhD Candidate Case Western Reserve University School of Medicine Cleveland, Ohio

Niloofar Farhang, BS

Graduate Research Assistant Department of Bioengineer ing University of Utah Salt Lake City, Utah

Fabio Galbusera, PhD

Head of the Laboratory of Biological Structures Mechanics IRCCS Istituto Ortopedico Galeazzi Milan, Italy

Edward C. Benzel, MD

Chairman, Department of Neurosurgery Neurological Institute Cleveland Clinic Cleveland, Ohio

Lawrence J. Bonassar, PhD

Professor Meinig School of Biomedical Engineering Sibley School of Mechanical and Aerospace Engineering Cornell University Ithaca, New York

Timothy Ganey, PhD

Director of Orthopaedic Research Atlanta Medical Center Atlanta, Georgia

Tony Goldschlager, MBBS, PhD, FRACS

Professor, Neurosurgeon Department of Surgery Monash University Melbourne, Victoria, Australia

Sibylle Grad, PhD

Principal Scientist Musculoskeletal Regeneration Program AO Research Institute Davos Davos, Switzerland

Contributors

Elliott A. Gruskin, PhD

Life Sciences Consultant Malvern, Pennsylvania

Peter Grunert, MD

Spine Fellow Swedish Neuroscience Institute Seattle, Washington

Lisbet Haglund, PhD

Associate Professor, Surgery The Orthopaedic Research Laboratory Montreal General Hospital Montreal, Quebec, Canada

Colin M. Haines, MD

Fellow Center for Spine Health Neurological Institute Cleveland Clinic Cleveland, Ohio

Roger Härtl, MD

Professor of Neurological Surgery Director of Spinal Surgery Director, Weill Cornell Medicine Center for Comprehensive

Spine Care Attending Neurosurgeon Weill Cornell Medicine, New York-Presbyterian Hospital New York, New York

Andrew C. Hecht

Chief, Spine Surgery Mount Sinai Health System Director, Spine Center Leni and Peter W. May Department of Orthopaedics Icahn School of Medicine at Mount Sinai New York, New York

Christian Hohaus, MD

Consultant Neurosurgeon Department of Neurosurgery BG Klinikum Bergmannstrost Halle, Germany

William C. Horton, MD

Vice President of Research & Development Franchise Medical Leader, Spine DePuy Synthes Spine Adjunct Professor of Orthopaedic Surgery The Emory Spine Center Emory University Atlanta, Georgia

Ibrahim Hussain, MD

Spine Fellow Weill Cornell Brain and Spine Center Department of Neurological Surgery Weill Cornell Medicine, New York-Presbyterian Hospital New York, New York

James C. Iatridis, PhD

Professor & Vice Chair for Research Mount Sinai Endowed Chair in Orthopaedic Research Director, Spine Research Program Leni and Peter W. May Department of Orthopaedics Icahn School of Medicine at Mount Sinai New York, New York

Kenji Kato, MD, PhD

Postdoctoral Fellow Department of Orthopaedic Surgery University of California, San Diego La Jolla, California

Gernot Lang, MD

Spine Fellow Weill Cornell Brain and Spine Center Department of Neurological Surgery Weill Cornell Medical College New York, New York

Brandon Lawrence, MD

Associate Professor Department of Orthopaedic Surgery University of Utah Salt Lake City, Utah

Victor Y. Leung, PhD

Research Assistant Professor Department of Orthopaedics & Traumatology The University of Hong Kong Hong Kong, SAR, China

Zhen Li, PhD

Research Scientist, Musculoskeletal Regeneration AO Research Institute Davos Davos, Switzerland

William Omar Contreras Lopez, MD, PhD

Professor Department of Functional Neurosurgery & Spine Surgery NEMOD International Neuromodulation Center UNAB Universit y Bucaramanga, Colombia

Contributors

Jeffrey C. Lotz, PhD

Professor and Vice Chair of Research DavidS.Bradford,MD,EndowedChairofOrthopaedicSurgery Department of Orthopaedic Surgery University of California San Francisco San Francisco, California

Keith D.K. Luk, MBBS, MCh(Orth), FRCSE, FRCSG, FRACS,

FHKAM(Orth)

Tam Sai-kit Professor in Spine Surgery Chair Professor and DivisionChief,Division of SpineSurgery Department of Orthopaedics & Traumatology The University of Hong Kong Pokfulam, Hong Kong

John T. Martin, PhD

Postdoctoral Researcher Department of Orthopaedic Surgery Duke University Durham, North Carolina

Koichi Masuda, MD

Professor Department of Orthopaedic Surgery University of California San Diego La Jolla, California

Robert L. Mauck, PhD

Mary Black Ralston Professor of Orthopedic Surgery Professor of Bioengineering Director, McKay Orthopaedic Research Laboratory Department of Orthopaedic Surgery University of Pennsylvania Philadelphia, Pennsylvania

Hans Jörg Meisel, MD, PhD

Director Centre of Neurosciences Chair Department of Neurosurgery BG Klinikum Bergmannstrost Halle, Germany

Yu Moriguchi, MD, PhD

Research Fellow Weill Cornell Brain and Spine Center Department of Neurological Surgery Weill Cornell Medicine, New York-Presbyterian Hospital New York, New York

Rodrigo Navarro-Ramirez, MD

Neurosurgeon Weill Cornell Brain and Spine Center Department of Neurological Surgery Weill Cornell Medicine, New York-Presbyterian Hospital New York, New York

Jean Ouellet, MD, FRCSC

Chair of McGill Scoliosis and Spine Centre Deputy Chief of Shriners Hospital Professor of Pediatric Surgery McGill University Health Centre Montreal, Quebec, Canada

Brenton Pennicooke, MD, MS

Neurological Surgery Resident Weill Cornell Brain and Spine Center Department of Neurological Surgery Weill Cornell Medicine, New York-Presbyterian Hospital New York, New York

Marianna Peroglio, PhD

Senior Research Scientist Musculoskeletal Regeneration AO Research Institute Davos Davos, Switzerland

Hollis G. Potter, MD

Chairman, Department of Radiology & Imaging The Coleman Chair, MRI Research Hospital for Special Surgery Weill Medical College of Cornell University New York, New York

Steven Presciutti, MD

Assistant Professor Orthopaedic Surgery Emory University Atlanta, Georgia

Michaela H. Purcell

Vice President, Clinical Affairs Isto Biologics St. Louis, Missouri

Timothy T. Roberts, MD

Fellow Center for Spine Health Neurological Institute Cleveland Clinic Cleveland, Ohio

Dike Ruan, MD

Chair Professor Department of Orthopaedics Vice Chairman Navy General Hospital Beijing, China

Contributors

Jaime Arias Ruiz, MD

NEMOD International Neuromodulation Center UNAB Universit y Bucaramanga, Colombia

Daisuke Sakai, MD, PhD

Associate Professor Tokai University School of Medicine Department of Orthopaedic Surgery Surgical Science Isehara, Kanagawa, Japan

Jordy Schol, BS

Tokai University School of Medicine Department of Orthopaedic Surgery Surgical Science Isehara, Kanagawa, Japan

Hassan Serhan, PhD

Distinguished Engineering Fellow, DePuy Synthes Spine Prestige Adjunct Professor Department of Bioengineering University of Toledo Toledo, Ohio

Stephen R. Sloan, Jr., BS

PhD Candidate Meinig School of Biomedical Engineering Cornell University Ithaca, New York

Harvey E. Smith, MD

Assistant Professor Department of Orthopaedic Surgery University of Pennsylvania School of Medicine Hospital of the University of Pennsylvania Veteran's Administration Medical Center Philadelphia, Pennsylvania

Lachlan J. Smith, PhD

Assistant Professor of Neurosurgery and Orthopaedic

Surgery Department of Neurosurgery University of Pennsylvania Philadelphia, Pennsylvania

Darryl B. Sneag, MD

Assistant Attending Radiologist Department of Radiology & Imaging, Hospital for

Special Surgery Assistant Professor of Radiology Weill Medical College of Cornell University New York, New York

Joshua Stover

University of Utah Salt Lake City, Utah

Claudius Thomé, MD

Professor and Chairman Department of Neurosurgery Medical University Innsbruck Innsbruck, Austria

Olivia M. Torre

PhD Candidate Leni and Peter W. May Department of Orthopaedics Icahn School of Medicine at Mount Sinai New York, New York

Julien Tremblay Gravel, MSc

Research Assistant McGill Scoliosis and Spine Centre McGill University Health Centre Montreal, Quebec, Canada

Luiz Vialle, MD, PhD

Professor of Orthopedics, School of Medicine Catholic University Spine Unit Curitiba, Brazil

Penny J. White

Vice President Emeritus, Regulatory and Quality Affairs Isto Biologics St. Louis, Missouri

Hans-Joachim Wilke, MD

Co-Director Head of Spine Research Institute of Orthopaedic Research and Biomechanics Trauma Research Center Ulm University Hospital Ulm Ulm, Germany

Micaella Zubkov, BS

Student Researcher Weill Cornell Brain and Spine Center Department of Neurological Surgery Weill Cornell Medical College New York, New York

xii

Part I

1 The Human Spinal Disc: Relevant

Anatomy and Physiology 2

Basics

2 Pathophysiology of Disc Disease: Disc

Degeneration 11

3 Imaging of the Healthy and Diseased

Spinal Disc 20

4 Biomechanics of the Healthy and

Diseased Spine 30

The Human Spinal Disc: Relevant Anatomy and Physiology

1 The Human Spinal Disc: Relevant Anatomy and Physiology

Julien Tremblay Gravel, Fahad H. Abduljabbar, Jean Ouellet, and Lisbet Haglund

Abstract The intervertebral disc (IVD) is a well-engineered avascular fibrocartilaginous organ designed to unite two adjacent vertebral bodies. Its anatomical and physiological properties provide constrained motion and force dissipation while maintaining the mechanical stability of the spine. The IVD is divided into two main sections: the annulus fibrosus (AF) and the nucleus pulposus (NP). The NP’s structure is of gelatinous consistency and has a high concentration of aggrecan and water that enable it to resist compression. As the spine is axially loaded, the forces are dissipated via the NP and the lamina of the AF.

Keywords: anatomy, biomechanics, intervertebral disc, spine

1.1 The Vertebral Column

The vertebral column is part of the axial skeleton; it is composed of 33 vertebral bodies that connect the skull base to the pelvis. It is divided into five regions: cervical (7 vertebrae), thoracic (12 vertebrae), lumbar (5 vertebrae), sacral (5 vertebrae), and coccygeal (4 vertebrae). The vertebral bodies are named in the cervical region C1–C7, in the thoracic region T1–T12, and in the lumbar region L1–L5. In the coronal plane the spine is straight, yet in the sagittal plane the spine has primary and secondary curves (▶ Fig. 1.1). The primary curvatures consist of the thoracic and sacral kyphosis. As we learn to sit and stand, the secondary curves take shape, giving rise to the cervical and lumbar lordosis. These cur ves are important for absorbing forces, maintaining balance, and allowing a range of motion throughout the vertebral column. Motion within the vertebral column varies between each spinal segment. The greatest freedom of motion is found in the cervical and lumbar segments and the most restrained motion is found in the thoracic and sacral segments as they are constrained by the ribs and pelvis. Each vertebra is composed of the vertebral body anteriorly and vertebral arch posteriorly. Each vertebral segment has a spinal canal and two intervertebral foramina, formed by the bony structures of the posterior arch. These structures provide a protected passage for the spinal cord and nerve roots, respectively. The vertebrae also serve as anchor points for the rib cage posteriorly, which helps protect the thoracic cavity organs. The vertebral arches have, posteriorly, two articulating synovial diarthrodial joints called facet joints. The facet joints’ surfaces are covered with articular cartilage and are enclosed by a synovial capsule. The facets prevent two adjacent vertebrae from translating during spinal motion, avoiding damage to the nerve roots and spinal cord. IVDs separate the upper 24 vertebral bodies, whereas the lower 9 are fused in adults. The IVDs and the facet joints provide the capacity for flexion and extension and to a lesser extent, rotation and lateral bending. Moreover, these facets share the load transmitted through the spine with the IVDs. The IVD is a fibrocartilaginous organ uniting two adjacent vertebral bodies, contributing to the spine’s height and function (▶ Fig. 1.2). The discs are named according to the upper and lower vertebrae they join. For example, the disc

situated between the thoracic vertebra T12 and the lumbar vertebra L1 is called T12–L1. The discs, in aggregate, make up approximately one fourth of the height of the spinal column excluding the sacrum and coccyx. essential for maintaining posture and for protecting delicate neural tissue and rigid structures of the vertebrae and skull during locomotion.

The human spinal disc is

1.2 Development of the Intervertebral Disc

The internal structure of the disc has distinct anatomical regions of diﬀerent developmental origin. These structures are traditionally separated into the central, gelatinous NP, the outer, fibrous AF, and the cartilaginous end plates.

Structures of the spinal column originate from the notochord and from the sclerotome of the mesodermal somites. There are four developmental stages to the formation of the vertebrae and discs. First, the notochord is formed from the mesoderm

Fig. 1.1 Schematic representation and anatomical regions of the human spine.

The Human Spinal Disc: Relevant Anatomy and Physiology

Fig. 1.2 Schematic representation and structure

of the human intervertebral disc and position within the human vertebral segment. Note the concentric arrangement of the annulus’ lamellae.

during gastrulation. It is positioned in the dorsal region of the embryo, along the anteroposterior axis. The notochord consists of a flexible core of glycoprotein with high osmotic potential

surrounded by a sheath of fibrous connective tissue.

During the second stage, at the 4th week of development, cells of the sclerotome migrate around the notochord forming the vertebrae, cartilaginous end plate, AF, and ribs. In the ventromedial region, the notochord is segmented. Some sections are remodeled to make way for the forming vertebral bodies, whereas others expand to form the NP, the gelatinous portion of the

The annulus is formed by a condensation of sclerotomal

IVD. cells surrounding the remaining sections of notochord. The condensation of these cells makes way for the expansion of the

notochordal tissue, forming the NP.

During the third stage, at 6 weeks, the vertebral parts of the spine undergo chondrogenesis and become cartilaginous (▶ Fig. 1.3). The fourth and final stage is ossification, which begins during the 8th week of the embryonic period and is completed around 25 years of age.

During fetal/early natal life, blood vessels penetrate the disc to the inner annulus. By the juvenile stage, the blood vessels resorb to the outer annulus and the cartilaginous end plates.

the nondegenerate adult disc, blood vessels are only seen in the connective tissue surrounding the AF and budding in the cartilaginous end plates. This lack of vascularity limits the flow of nutrients reaching the central region of the disc. Nerves follow

a similar pattern, penetrating only the outer AF in nondegenerate adult discs (▶ Fig. 1.4, ▶ Fig. 1.5).

1.3 Cells in the Intervertebral Disc

The overall cell density of the disc is fairly high in the fetal stage but decreases significantly with age, especially in the regions furthest from the periphery.

Cells of the NP are notochordal in origin. are large (> 15µm) and contain large vacuoles, NP cells are relatively small (10 um diameter) and display a rounded chondrocyte-like morphology. Multiple studies have demonstrated that cells of the mature human NP express distinct notochordal markers, such as brachyury, further establishing the notochord as the developmental origin of NP cells. The vacuoles of notochord cells carry a multitude of anabolic factors suggested to induce matrix synthesis in neighboring cells. Notochordal cells disappear with age and are no longer

visible by the age of 4 in humans. tion of these cells may therefore contribute to age-related tissue

Loss or terminal diﬀerentia-

deterioration. NP cells are situated in lacunae and do not con-

tain vacuoles.

They are sparsely and randomly distributed within the tissue, with a cell density of about 4,000 cells per mm

in the adult.

6,7

Notochordal cells

whereas mature

8,9

The Human Spinal Disc: Relevant Anatomy and Physiology

Fig. 1.3 Schematic representation of intervertebral disc development. At 22 days postconception the notochord forms on the ventromedial aspect of

the embryo, elongating along its craniocaudal axis. The neural groove closes to form the early spinal cord, positioned dorsally to the notochord along the same axis. These structures are flanked on each side by a row of somites. At 30 days postconception sclerotomal cells of the somites separate from myotomal cells and migrate around the notochord toward the midline. At the 4th to 6th embryonic week sclerotomal cells aggregate around the notochord and spinal cord. Segments of alternating high and low sclerotomal cell density form, giving rise to the early annulus fibrosus and vertebral bone, respectively. At the 7th to 9th embryonic week sclerotomal cells of the early vertebral bone expand, pushing away the notochord from the center of the vertebral body. Simultaneously, cells of the early annulus condense to allow space for the notochordal tissue exiting the vertebral body, giving rise to the nucleus pulposus region.

Annulus cells originate from the sclerotome, and are elongated and spindle shaped. They are arranged following the lamellae’s orientation. Their diameter varies between 15 and

30 µm. 9,000 cells per mm

The AF is more densely cellularized, with about

in the adult human.

The cells in the end plate cartilage are chondrocytes of mesenchymal origin. Like in the deep layers of articular cartilage, the chondrocytes are situated in lacunae arranged in a columnar fashion. The end plate has the highest cell density of any

3.10

disc tissue, with approximately 15,000 cells/mm

age diameter is 20 µm

(▶ Fig. 1.6).

Their aver-

The Human Spinal Disc: Relevant Anatomy and Physiology

Fig. 1.4 (a) Vascular network of the vertebral body and intervertebral disc in the newborn; vessels reach into the inner region of the annulus fibrosus (AF). (b) Juvenile vessels recede to the outer region of the AF. (c) Adult vessels are restricted to the end plate and connective tissue surrounding the AF.

NP, AF, and cartilage end plate cells are, in addition to matrix synthesis, responsible for maintenance and turnover of the extracellular matrix (ECM), a process that is in balance in the young and nondegenerate disc.

1.4 Intervertebral Disc Organization and Composition

The disc’s distinct anatomical regions have diﬀerent mechanical and biological properties. The AF and NP regions are clearly distinguishable in fetal and juvenile discs but the clear demarcations diminish in the adult. The NP region expands in the adult disc into a transition region called the inner AF, and it can be diﬃcult to establish where one region begins and the other ends (▶ Fig. 1.2). The tissue regions contain similar matrix elements, albeit in widely diﬀering concentrations.

The disc’s

ECM is rich in collagen and proteoglycan. Collagen is a ubiquitous protein in mammalian connective tissue. Diﬀerent types of collagen are present in varying amounts within the disc, but the most prominent by far are types I and II. Other collagens present within the mature, nondegenerate disc are types III, V, VI, IX, XI, XII, and XIV. cells and a three-dimensional (3D) mesh confining other matrix elements, such as proteoglycans. Proteoglycans exist in two forms within the disc, either bound to hyaluronic acid or unbound. The most abundant proteoglycan within the disc is aggrecan. In early development stages, most aggrecan within the disc is bound to hyaluronan, with a shift toward unbound forms in later stages of development. Other proteoglycans found in the disc’s ECM are versican and members of the small leucine rich protein (SLRP) family: chondroadherin, decorin, fibromodulin, and lumican. defined functions in the tissue and most of them carry

Collagen provides attachment to disc

The SLRPs have many

The Human Spinal Disc: Relevant Anatomy and Physiology

Fig. 1.5 The sinuvertebral nerve originates near

the vertebral segment to innervate the disc. Nerve endings rarely penetrate beyond the outer layer of the annulus fibrosus in a nondegenerate adult disc.

glycosaminoglycan (GAG) chains. Chondroadherin is one of the few without GAG chains; it anchors the cells to the ECM via

16,17,18

integrin and syndecan receptors.

Decorin, fibromodulin, and lumican carry GAG chains. Decorin cross-links collagen fibers, whereas fibromodulin and lumican have highly negative sulfated tyrosine domains that bind cytokines and matrix

18,19,20

metalloproteinases.

Proteoglycans are made up of a core protein to which o ne or more GAG chains of highly sulphated repeating disacc haride units are covalently attached. Most proteoglycans have 1 or 2 GAG chains, whereas aggrecan has up to 150.

1.4.1 Nucleus Pulposus

The NP’s structure is gelatinous and has high aggrecan content. This molecule’s many GAG chains contr ibute to water retention and provide swelling pressure through their fixed negative charges. Aggrecan is the greatest contributor to NP function by enabling it to resist compression. Aggrecan concentration is highest in the central portion of the NP and declines throughout the AF. The other matrix molecule primarily responsible for the mechanical function of the NP is collagen type II. Collagen provides a scaﬀold entrapping aggrecan and other molecules and provides tensile properties to the tissue. Collagen and aggrecan make up 20% and 50% of the NP’s dry weight, respec-

tively. properties of cartilage. However, the ratio of aggrecan to collagen is 2:1 in cartilage, whereas it is 27:1 within the NP. Although aggrecan represents 50% of the dry weight, 70 to 90% of the NP’s wet volume is occupied by water bound to

The same molecules are responsible for the mechanical

aggrecan.

The high proteoglycan content with its negative charge is also thought to be a major factor preventing nerve ingrowth into the largely aneural and avascular mature, nonde-

24,25

generate IVD.

Peripherally, the NP is encircled by the AF.

1.4.2 Annulus Fibrosus

The function of the AF is to restrict lateral motion, as well as to prevent extrusion, of the nuclear material. To accomplish this, the collagen fibers of the mature annulus are arranged in up to 25 concentric lamellae wrapped around the NP. The lamellae are parallel to one another traversing between adjacent vertebrae at an angle of 60 degrees to the axis of the spine (▶ Fig. 1.2). The collagen fibers within a single annular lamella are organized in a parallel fashion, whereas the fibers in adjacent layers diﬀer by 30 degrees. type I is highest in the annulus and decreases radially toward the NP. Collagen type II follows an inverse pattern with the highest concentration in the NP.

Proteoglycans, such as aggrecan, are present throughout the AF but at a concentration much lower than in the NP. Collagen makes up 50 to 70% of annular tissue dry weight and proteoglycans only 10 to 20% of dry weight. network between the lamellae, contribute to the structure and mechanical functions of the AF.

1.4.3 Vertebral End Plate

The vertebral end plate has a dual function. It anchors the disc to the vertebrae and provides the main avenue for nutrient and

The concentration of collagen

Elastin fibers, arranged in a

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